J Pest Sci DOI 10.1007/s10340-014-0583-5

ORIGINAL PAPER

IPM thresholds for wireworm species in maize in Southern Europe

Lorenzo Furlan

Received: 3 November 2013 / Accepted: 16 March 2014 Ó The Author(s) 2014. This article is published with open access at Springerlink.com

Abstract Currently, integrated pest management (IPM) Keywords Wireworms Á A. brevis Á A. sordidus Á of wireworms is not widespread in Europe. Therefore, to A. ustulatus Á IPM Á Bait traps estimate the densities of three major wireworm species in southern Europe (Agriotes brevis Candeze, A. sordidus Il- liger, and A. ustulatus Scha¨ller), bait traps were deployed Introduction pre-seeding in maize fields in north-eastern Italy between 1993 and 2011. Research discovered that there was a sig- EU Directive 2009/128/EC on the sustainable use of pes- nificant correlation between all three wireworm species ticides makes it compulsory to implement integrated pest caught in the bait traps and damage to maize plants, but management (IPM) for annual crops in Europe from Jan- damage symptoms varied. Wherever A. ustulatus was the uary 2014. IPM strategies have not played a significant role main species caught, there was no significant damage to in these crops to date, yet they have been widely used for maize plants, but seeds were damaged. Most of the crops such as orchards and vineyards. Therefore, accurate symptoms caused by A. brevis and A. sordidus were to the information about IPM strategies for annual crops is nee- central leaf/leaves, which wilted because of feeding on the ded urgently, but this information must take into account collar. A. brevis was the most harmful species; when more that arable farming has few resources in terms of income, than one A. brevis wireworm was caught per trap, plant labour and technology. Since the use of soil insecticides is damage sometimes resulted in reduced yield. Five A. widespread, this paper intends to provide reliable IPM ustulatus larvae per trap caused the same damage to maize information to tackle wireworms, the main soil pest in as one A. brevis. A. sordidus came second (threshold two Europe (Furlan 2005). It has proved difficult to implement larvae/trap). These thresholds are reliable for: (1) bare soil IPM strategies for wireworms in Europe due to a shortage in which there are no alternative food sources; (2) average of reliable information on how to assess population levels soil temperature 10 cm beneath the surface of above 8 °C and the relative thresholds (Furlan 2005). Wireworms are for 10 days; (3) soil humidity near to field water capacity, the larvae of click (Coleoptera: Elateridae), but but days of flooding have not been considered. The damage-causing genera and species vary with geographic implementation of the practical method described herein location (Furlan et al. 2000, 2001b, 2007a; Rusek 1972; may lead to effective IPM of wireworms in maize and to a Staudacher et al. 2013). In Europe, most larvae in agri- significant reduction in the number of fields treated with cultural land belong to the Agriotes genus, but the specific soil insecticides. species must be established if we are to predict the potential damage to crops. For example, high populations of Agriotes ustulatus do not damage maize late in the Communicated by M. Traugott. spring (late May–June) because most of the larvae are in a non-feeding phase (Furlan 1998); in the same period, & L. Furlan ( ) however, Agriotes sordidus or A. brevis can seriously Veneto Agricoltura, Agripolis, via dell’Universita` 14, Legnaro, PD, Italy reduce the stand of maize crops (Furlan 2004). The adults e-mail: [email protected] (click beetles) of these species can be divided into two 123 J Pest Sci main groups: (i) adults that do not overwinter and lay eggs accordance with official USDA methods. Soil pH was basic a few days after swarming (A. ustulatus Scha¨ller and A. for all the fields and ranged between 7.9 and 8.3. litigiosus Rossi); and (ii) adults that overwinter, live for months, and lay eggs for a long period after adult hard- Agronomic practices ening (A. sordidus Illiger, A. brevis Candeze, A. lineatus L., A. sputator L., A. obscurus L., A. rufipalpis Brulle`, and A. Conventional agronomic practices were applied to all of the proximus Schwarz) (Furlan 2005). The life cycle of the fields studied (i.e. ploughing, harrowing, fertilization with species in both groups is about 24–36 months. In spring, 240–300 N kg, 70,000–76,000 seeds/ha, interrow width the larvae of group (i) entering the bait traps come from 75 cm, pre-emergence plus post-emergence herbicide eggs laid two years before, but group (ii) larvae come treatments causing very low weed densities, and planting mainly from eggs laid the previous year. Unfortunately, the date from late March to late April). The following com- vast majority of literature on this matter does not report mercial hybrids were used: ANITA, COSTANZA, ALICIA, which species were involved (Hinkin 1976; Chabert and SENEGAL (1993–2001); TEVERE (2002–2004); Blot 1992). Therefore, this present research assesses the DKC6530 (2005–2006); DKC 6530, MITIC, KERMESS, effect of various Agriotes species on maize and looks at KLAXON (2007–2008); DKC6666, NK FAMOSO, thresholds based on wireworms caught in bait traps in order PR31A34, PR32G44 (2009–2010); and DKC6677, to establish a range of IPM strategies. The ultimate aim of PR32G44 and NK FAMOSO (2011). the research is to provide practical information so that European farmers can implement reliable, feasible and Estimation of wireworm population level affordable IPM strategies to prevent wireworms damaging their maize. Bait traps made and used in accordance with Chabert and Blot (1992) were deployed to estimate wireworm popula- tion densities from late February to mid April. These and Materials and methods similar traps were found to be efficient at capturing wire- worms after research in UK conditions (Parker 1994, Field sites 1996). Each trap comprised a plastic pot 10 cm in diameter with holes in the bottom. The pots were filled with ver- Research was conducted in north-east Italy (area covered: miculite, 30 ml of wheat seeds and 30 ml of maize seeds; 45.64N, 12.96E and 45.05N 11.88E) from 1993 to 2011 they were then moistened before being placed into the soil (19 consecutive years) on fields with the following char- 4–5 cm below the soil surface, after which they were acteristics: (1) soil at field water capacity, i.e. no more covered with an 18-cm diameter plastic lid placed 1–2 cm water can be stably retained; after winter, all of the fields above the pot rim. Traps were hand-sorted after 10 days studied, and particularly the bare ones, i.e. no crops con- when the average temperature 10 cm beneath the surface suming water, are usually very humid due to rainfall, was above 8 °C (Furlan 1998, 2004) to ensure that the bait negligible evaporation and transpiration. Sometimes strong traps stayed in the soil for an equal period of wireworm winds dried up the soil, but only the top-most layer and not activity. Agriotes larvae do not feed, or feed very little, at where the traps were placed. Therefore, the soil layer lower temperatures. Generally, the traps were removed containing the traps was always at field water capacity; (2) from the fields 2 to 8 days before maize seeding. No bare soil (no plants growing), since traps perform reliably considerable differences in wireworm feeding activity were when they do not have to compete with plants whose roots observed between 8 and 13 °C, which is the usual tem- produce carbon dioxide, which attracts larvae (Doane et al. perature range in early spring in northern Italy (Furlan 1975); (3) several previous crops had been sown, such as 1998, 2004). Previous investigations (unpublished data) maize, soybean, winter cereals and meadow (e.g. alfalfa, found that only a negligible number of larvae escaped from festuca); meadow must be ploughed at least three months the traps since it was noted that numbers tended to increase before the bait traps are placed in order to make sure that as days passed (Furlan personal observation). The final all ploughed-up meadow plants have died (it was observed number of larvae was assessed under the aforementioned that this takes about three months); the main reason for this conditions, regardless of larvae behaviour on individual procedure is that it allows the bait traps to attract wire- days. Population levels were calculated only on days when worms without the competition of plants, as described humidity was close to field water capacity. Dry top-soil above. Each year, monitoring was conducted in fields forces larvae to burrow deep beneath the surface, away representing a balanced sample of agronomic conditions in from the bait traps (Furlan 1998), and high humidity north-east Italy. Part of the soils was classified with the (flooding in extreme cases) prevents larvae activity since USDA soil texture triangle based on analyses carried out in all the soil pores are full of water and contain no oxygen. 123 J Pest Sci

Therefore, any days on which these conditions occurred were counted; the plots covered an area of were excluded from calculations, regardless of the soil 15–18 m 9 1.5 m. The location and the number of the sub- temperature. This obviously resulted in traps sometimes plots were the same in both the untreated/treated strips and being kept in the soil for longer than 10 days. In the UK, completely untreated field. In order to assess wireworm Parker (1994) caught large numbers of Agriotes wireworms damage on emerged plants, plants with typical symptoms in average soil temperatures that ranged from 5 to 10 °C. In (e.g. wilting central leaves, broken central leaf due to holes order to recover as many larvae as possible, and thus in the collar, wilting of whole small plants) were sought increase research precision, after 10 or more days, the traps and the soil around the plants was dug up to a depth were inspected manually and the contents put into Berlese 5–6 cm; any larvae found near the collar were collected funnels fitted with a 0.5-cm mesh screen at the bottom. The and identified. Wherever maize plants were missing from trap contents were allowed to dry for at least 20 days in a the rows, the soil was dug up in order to assess possible sheltered place without lamps, and the larvae that fell into wireworm damage to seeds and/or emerging seedlings. the collecting vials were counted and identified. A personal Total plant damage was calculated as the sum of damage to key (unpublished), developed by rearing single larvae to emerged plants and seeds. In order to establish the effect of adults, was used to identify them. Some of the distin- wireworm damage on yield, the same observations were guishing characteristics complied with Rudolph (1974). made on the treated strips/plots where used. Finally, the Adults were determined with the key in Platia (1994). The strips and the plots were harvested and the maize grain traps were deployed on a grid (20 m 9 10 m apart); a weighed. Maize grain samples were collected and their minimum of nine bait traps was placed per field and the humidity measured with a Pfeuffer-Granomat (the same sample area varied between 0.2 and 1 ha. The larger the machine was used for all samples each year). The four area to be covered, the higher the number of traps placed. A fields in which maize stands were irregular and damaged total of 5,400 traps were placed during this 19-year study due to factors other than wireworm activity (e.g. bird (18 traps/field on average). This research encompassed damage, low emergence due to low soil moisture, flooding) only fields monitored in spring (early March to late April). were not considered. In order to isolate the ‘‘wireworm damage effect’’, analysis excluded the two fields under Estimation of wireworm damage to maize considerable pressure from factors other than wireworms (e.g. other parasites, viruses). Fields in which the general In the maize fields monitored, wireworm damage to seeds conditions were good, but the soil insecticide had not and plants was assessed only once it was sure that insec- worked completely and the stand of treated maize plots was ticides had not been used, or that random untreated maize not optimal, were not used to evaluate the effect on yield strips/plots, 3 or 4.5 m wide, had been sown alternately (this happened in two cases only). In the remaining fields with treated strips/plots. When strips/plots were treated, the where the insecticides had worked effectively, the final most effective insecticides available were used: stand of the treated strips/plots was suitable for assessing 1993–1994: DiphonateÒ (Fonofos 4.75 % a.i.) 10 kg/ha of whether yield had been reduced ([90 % of the sown granules applied in-furrow; DotanÒ (Chlormephos 4.95 % seeds). a.i.) 7 kg/ha of granules applied in-furrow; 1995–2005: Fipronil (Regent TSÒ) 0.6 mg a.i./seed; Imidacloprid Statistical methods (GauchoÒ) 1.2 mg a.i./seed; Regent 2GÒ (Fipronil 2 % a.i.) 5 kg/ha of granules applied in-furrow; 2006–2010: All analyses were performed by SAS 9.3 (SAS Institute ForceÒ ST (Tefluthrin 0.5 % a.i.) 15 kg/ha of granules Inc., Cary, NC). Linear regression analysis was used to applied in-furrow; Clothiadinin (PonchoÒ) 0.5 mg a.i./ determine the relationship between damage to maize (total seed; 2011: ForceÒ ST (Tefluthrin 0.5 % a.i.) 15 kg/ha of plant damage, emerged plant damage and seed damage) granules applied in-furrow; Clothiadinin (PonchoÒ) and pre-seeding catches of wireworms in bait traps for each 0.5 mg a.i./seed; Imidacloprid (GauchoÒ) 1.2 mg a.i./seed. species. A paired t test was used to assess the effect of One litre of the fungicide Metalaxil ? Fludioxonil wireworm damage on grain yields in treated and non- (CelestÒ) per tonne of seed was used to treat all of the treated plots. Where soil characteristics were available, a maize seeds planted. In order to study the correlation generalized linear model (Nelder and Wedderburn 1972) between wireworm densities (larvae/bait trap) and the with a Poisson distribution was used to determine the damage to maize, at the 2–3 and 6–8 leaf stages, two sub- factors affecting the percentage of total damage for each plots of 4 9 20 m rows of maize per portion of untreated species. The model included the effect of the main agro- field (0.1–0.2 ha) or untreated strip were chosen at random nomic characteristics (soil texture as a fixed effect, plus and the plants observed. During plot trials, all plants organic matter content and pH as covariates) and captures/ (healthy and damaged) at the centre of each untreated plot plant damage data (as covariates too). The soil types (levels 123 J Pest Sci

Table 1 Wireworms found in Species Fields the fields monitored with bait traps pre-seeding; fields are Total One Agriotes brevis ? Agriotes brevis ? Agriotes sordidus ? All three divided in accordance with the species Agriotes sordidus Agriotes ustulatus Agriotes ustulatus species number of species found in each one Fields (no.) 206 167 9 8 12 10 A. brevis larvae 2,431 1,959 89 197 0 186 A. sordidus larvae 1,486 1,353 85 0 30 18 A. ustulatus larvae 4,217 3,765 0 160 280 12

of the variable) were classified as follows: clay, loam, clay texture affected the risk: loam soils were prone to higher loam, silt clay loam, loam, sandy loam, and loamy sand. damage risk by A. sordidus, while the risk of damage by A. Analysis produced least squares means estimates of ustulatus was much lower in clay soils. PH variations in the parameters and risk ratio. Risk ratio measures relative range of soils studied (mean = 8.01, SD = 0.11) did not effect expressed by the outcome in two groups, i.e. the ratio influence the risk of damage by any of the species, but between the prevalence in the exposed group (numerator organic matter content (mean = 1.93, SD = 0.49) may level) vs the non-exposed group (denominator or reference vary the risk of damage by A. ustulatus (Table 3, value). The type of soil with the highest damage level P \ 0.001). caused by each species was chosen as reference value. Analysis was performed with PROC GENMOD. The correlation between species caught by bait traps and symptoms observed on maize plants

Results Symptoms on maize plants varied per wireworm species. Wherever A. ustulatus was the prevalent species, no sig- Species composition and factors affecting the level nificant symptoms were found on emerged maize plants of damage (e.g. wilting central leaves); see Table 5 and Fig. 1. Symptoms on emerged plants were always caused by A. Wireworms were found in the bait traps in 206 fields brevis and/or A. sordidus (Table 2; Fig. 1). Only one case (70 %). The main species found were A. brevis, A. sordidus of serious seed damage by A. brevis was observed; the and A. ustulatus. All of these species are widespread in maize had been sown late and the seeds germinated in May central and southern Europe (Furlan 1996, 2004; Furlan due to a prolonged dry spell. No significant seed damage by et al. 2000, 2007a; Kausnitzer 1994) including areas with A. sordidus larvae was observed. A. ustulatus larvae significantly different conditions from those of this study, (Table 5) significantly affected plant stand by damaging e.g. in Austria, A. brevis were found in zones with acid pH seeds, which could not germinate or emerge when the (Staudacher et al. 2013). The presence of other Elateridae population was high. Few maize plants had the central leaf species (mainly Synaptus filiformis Fabricius, Melanotus broken by A. ustulatus feeding below ground; in the fields spp., rachifer Geoffroy in Fourcroy) was negli- where A. ustulatus was the prevalent species, less than gible. Bait traps caught a single species in 81.1 % of the 0.1 % of plants were damaged (3 out of a total of 3,100 fields. The combinations of different species observed in seeds ? plants found damaged). Broken central leaves the other cases are described in Table 1. Only four fields were restricted to the 3–4 leaf stage. A. brevis and A. (1.9 %) had a considerably mixed population (two or three sordidus proved able to cause all of the possible symptoms species in a single bait trap). Table 2 covers the fields in and to damage even developed maize plants (up to the 8–10 which at least one trap caught wireworms and gives the leaf stage). Most of the damaged plants had one or more average, standard deviation and maximum value of all the wilted central leaves due to larval feeding on the collar, single averages, standard deviations and maximum num- which sometimes killed them. bers estimated in each of the fields monitored. The vari- ability between bait traps was high, and the ratio between The correlation between species caught by bait traps average mean and average standard deviations was one. and damage to maize The generalized linear model found that the percentage of total damage variability was mainly explained by wire- All or most of the larvae collected from damaged seeds, worm density (the average number of larvae/bait trap) for seedlings or plants belonged to the prevalent species captured all three of the species studied (Table 3, P \ 0.001). Soil by the bait traps (Table 4). A significant correlation (for all 123 J Pest Sci

Table 2 Variability between the number of wireworms in the single bait traps placed in fields monitored Agriotes brevis Agriotes sordidus Agriotes ustulatus Mean SD Max Mean SD Max Mean SD Max

Mean 0.61 0.41 1.50 0.38 0.49 1.60 1.04 1.13 4.11 SD 3.27 1.71 6.43 0.65 0.61 2.05 3.25 2.88 10.58 Max 24.88 14.18 53 3.58 2.99 9 21.80 17.51 60 Average, standard deviation (SD) and maximum value of the all averages, standard deviations and maximum numbers calculated per each of the fields monitored. Only fields with average higher than zero have been considered (Agriotes brevis 48 fields, Agriotes sordidus 103 fields, Agriotes ustulatus 55 fields)

species) was discovered between the average number of attacked and, in most cases, they partially or completely wireworms caught in bait traps and the total damage to maize recovered. In some cases, damage of over 1 plant/m2 led to (damage to seeds, plus damage to emerged plants; Table 5, significant yield reduction (Fig. 1). Nevertheless, in others, Fig. 1). A. brevis was the most harmful species, as even even very severe plant damage ([3plants/m2;[40 %) did not wireworm densities just over one wireworm/trap caused result in reduced yield. For example, in the same year (2011), considerable plant damage (one to two plants attacked/m2), severe plant damage ([3plants/m2;[50 %) resulted in sig- i.e. enough to reduce yield (Fig. 1;Table 6). The graph shows nificant yield reduction at one site, but another trial produced either a very low or a high population (only three fields had a no difference between untreated plots (8.74 t/ha) and Imida- very high population) and almost nothing in between. During cloprid-treated plots (8.59 t/ha), despite the treated plots this 19-year research, high A. brevis populations were found in giving much higher stands than untreated ones in both trials. maize fields after meadow had been ploughed, or after a soil Plant damage below 1 plant/m2 never resulted in significant had been continuously covered with vegetation (e.g. soybeans yield reduction, and there were very limited differences just after winter-wheat in the same growing season). After the (ranging between 0.01 and 0.3 t/ha) between treated and first year of maize, the wireworm populations decreased dra- untreated strips or plots (see Furlan et al. 2002, 2007, 2009a, b, matically; this means that high populations are possible, but 2011). The 2011 study confirmed the previous long-term uncommon, as they occurred only in a few meadows and fields observations (Table 7). A further field infested by A. brevis where crops were continuously planted. Low populations, (damage [3plants/m2; [50 %) experienced a significant however, were common, as levels fell the very nextspring, and yield reduction of 4.2 t/ha. The hybrid was PR32G44. usually remained low for several years after. Intermediate Wherever wireworm densities of A. ustulatus were lower than populations are therefore rare. To cause the same level of five larvae/trap and A. sordidus were lower than two larvae/ damage in maize fields, five times more A. ustulatus larvae are trap (Fig. 1), stand reduction was lower than 0.5 plants/m2 (in needed (Fig. 1;Table 6). In Fig. 1, the notable outlier in the A. most cases, less than 5 % oftotal plants); no fields experienced ustulatus graph concerns a 2010 trial; the results may be reduced yield (i.e. there were no significant differences explained by a cold spring and a very compact soil, which between treated and untreated strips/plot (Table 6; Fig. 1). significantly slowed the emergence of maize seedlings, leav- ing them in the soil for a long time (about 20 days). These soil and climatic conditions did not cause significant damage in Discussion other fields with lower wireworm populations. A. ustulatus caused almost identical total damage and seed damage This long-term research found a significant correlation because it harmed very few emerged plants; on the contrary, between the number of wireworms caught in bait traps very few maize seeds were damaged by A. brevis and A. before seeding and damage to maize plants caused by three sordidus. A. sordidus was the second most harmful with of Europe’s main wireworm species: A. brevis, A. sordidus wireworm densities above two larvae/trap leading to reduced and A. ustulatus. Over the last 19 years, whatever the yield (Fig. 1;Table6). In Fig. 1 (A. sordidus), the outlier hybrid, and regardless of agronomic and climatic condi- fields, which experienced a significant decrease in yield, had tions, no yield reduction was observed when A. brevis sandy loam soils. Similar population levels did not cause populations were lower than one larva/trap, A. sordidus serious damage in heavy soils. In most fields (0–1 larva/trap), populations were lower than two larvae/trap and A. ustul- wireworm damage was negligible and did not cause any vis- atus populations were lower than five larvae/trap. These ible effects on maize crops, i.e. less than 5 % of plants were should be considered reliable thresholds for each species.

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Table 3 Least squares means Variable Number of Least squares means RR (95 % CI) Chi-square P (% of total damage on plants) fields % Damage (SE) and risk ratio for Agriotes ustulatus, Agriotes sordidus and Agriotes ustulatus Agriotes brevis in different soils Soil 25.96 \0.001 and different pH levels, percentage of organic matter Clay 7 0.27 (0.12) 0.22 (0.19–0.25) 12.86 \0.001 and number of larvae/trap Loama 31 1.24(0.23) calculated with a generalized Clay loam 3 0.08 (0.13) 0.06 (0.002–1.78) 2.62 0.105 linear model pH – – – Organic matter (%) 2.04 (1.23–3.39) 7.53 \0.001 No. larvae/trap 1.25 (1.21–1.28) 455.42 \0.001 Agriotes sordidus Soil 67.50 \0.001 Silty clay loam 2 1.37 (1.08) 0.35 (0.07–1.67) 1.74 0.187 Loam 9 1.30 (0.44) 0.33 (0.16–0.67) 9.29 0.002 Clay loam 15 0.63 (0.19) 0.16 (0.09–0.29) 36.05 \0.001 Silty clay loam 12 2.18 (0.63) 0.55 (28–1.06) 3.16 0.076 Sandy loam 9 2.29 (0.52) 0.58 (0.36–0.93) 5.07 0.024 Loamy sanda 32 3.96 (0.46) pH 0.24 (0.03–2.22) 1.50 0.221 Organic matter (%) 0.59 (0.25–1.37) 1.74 0.188 No. larvae/trap 1.96 (1.74–2.21) 106.19 \0.001 Agriotes brevis Soil Clay 11 11.73 (1.19) 0.55 (0.32–0.94) 4.78 0.029 Loam 4 2.84 (1.13) 0.13 (0.04–0.40) 12.69 \0.001 Clay loam 8 8.45 (1.26) 0.40 (0.23–0.67) 11.96 \0.001 a RR risk ratio,SEstandard error, Loamy sand 2 21.36 (5.58) CI confidence interval pH 15.40 (0.29–[20) 1.82 0.178 a Represents the reference level Organic matter (%) 1.27 (0.56–2.88) 0.32 0.569 of comparison in the calculation No. larvae/trap 1.07 (1.06–1.09) 128.49 \0.001 of risk ratio

Populations were assessed via the deployment of at least bait traps are placed (no other previously grown crops have nine bait traps in a sample soil grid (20 m 9 10 m). any particular requirements); (ii) average soil temperature Although statistical analyses show that much of the vari- 10 cm beneath the surface is above 8 °C for 10 days ability in wireworm plant damage cannot be explained by (including non-consecutive days); soil humidity is near to the wireworm densities estimated by the bait traps, i.e. high field water capacity, but days when soil humidity is over wireworm density does not always mean high damage, this water capacity (soil pores filled with water, i.e. flooding) study did demonstrate that serious plant damage resulting are not to be considered, regardless of soil temperature, in yield reduction may only occur when wireworm popu- since the wireworms are not active. These can be consid- lations are above the thresholds established above, pro- ered reliable, prudent economic thresholds for the imple- vided that precise conditions occur. mentation of IPM in maize in Italy and probably in the countries where the studied species are present in similar Conditions needed to use the thresholds agronomic and climatic conditions. When trap catches are below the established thresholds, the probability of eco- In order to use the thresholds established, the following nomic damage is negligible. However, although significant conditions have to be satisfied: (i) no alternative food yield reduction is a risk when thresholds are exceeded, it sources are available, soil is bare, and if meadow (e.g. may not always occur, as a combination of climatic and alfalfa, festuca) has been cultivated previously, the field agronomic factors (e.g. hybrid, soil, rainfall, fertilization, must have been ploughed at least three months before the irrigation) may compensate for stand reduction. In most

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cases, yield did not fall. Several factors may influence trap catches, including: (i) alternative food sources (Parker 1996); (ii) soil temperature (Furlan 1998, 2004; Chabert and Blot 1992); and (iii) soil moisture usually suitable for wireworm activity in spring in Italy and many other European countries. Thresholds, however, do need to be evaluated for different species and, for the species con- sidered in this manuscript, under other conditions.

Practical implementation of thresholds

Thresholds expressed as the number of wireworms per m2, or per trap, that do not specify the species caught (e.g. Hinkin 1976) do little to help IPM. Chabert and Blot (1992) suggest one wireworm/trap as a threshold for early planted maize based on their observations in northern France. Their work, however, does not discriminate the larvae captured and provides no statistics. From a practical point of view, the prevalent A. species in fields intended for maize crops need to be identified if the correct IPM thresholds are to be established. This could be achieved by: (a) a quick bin- ocular observation of representative larvae samples col- lected from fields (this needs trained people; currently a trained technician can identify about 40 larvae/h); (b) PCR- based identification (Ellis et al. 2009; Staudacher et al. 2010); and (c) indirectly evaluating: (i) information from click monitoring with pheromone traps (Furlan et al. 2001a; Furlan and To´th 2007;To´th et al. 2003) since captured click beetles may be correlated with the presence in the soil of same-species larvae, at least for the three main species considered herein (Furlan et al. 2001b) while this is uncertain for other important European species, such as A. obscurus L., A. lineatus L. and A. sputator L. (Benefer et al. 2012; Blackshaw and Hicks 2013; Landl et al. 2010); and (ii) the characteristics of the field (Blackshaw and Hicks 2013; Furlan et al. 2011; Hermann et al. 2013; Staudacher et al. 2013). From a practical point of view, when a restricted area is monitored, the main Agriotes species can be easily determined because the number of the main species is limited, and a trained IPM technician can therefore identify the larvae of the few species present based on their few discriminating characteristics. Further- more, when field information (e.g. rotation, captures) is collected and mapped properly, technicians will only need to determine a few larvae to garner reliable information about the species involved, as the species in a Fig. 1 The relationship between wireworm density (number of field tends to remain the same for at least about 4–5 years if 2 wireworms/bait trap) and total plant damage (plants/m ) for Agriotes conditions remain unchanged (Furlan, personal observa- ustulatus, A. brevis and A. sordidus (±95 % average confidence level). Larger (rhomb) dots represent combinations that resulted in a tion). Further studies on the agronomic factors influencing significant yield reduction crop response to wireworm damage (e.g. hybrids com-

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Table 4 Wireworm species identified as damaging maize seeds and plants in fields monitored with bait traps expressed as a percentage of the total number of larvae collected from damaged plants Fields (no.) Species in bait traps Agriotes ustulatus Agriotes brevis Agriotes sordidus Others Total number of larvae

30 Agriotes ustulatus 99.5 0.2 0.2 0.1 1,015 31 Agriotes brevis 0.1 99.6 0.2 0.1 754 88 Agriotes sordidus 0.1 0.2 99.7 0.0 622 This table considers only fields where bait traps caught larvae belonging to one species

Table 5 Statistical outputs of the linear relationships between damage to maize and pre-seeding catches of wireworms (Agriotes brevis, Agriotes sordidus, Agriotes ustulatus) in bait traps Fields (no.) Species Total plant damage (plants/m2) Seed damage (n/m2) Emerged plant damage (plants/m2) R2 P R2 P R2 P

69 Agriotes brevis 0.621 \0.0001 0.002 0.709 0.610 \0.0001 135 Agriotes sordidus 0.380 \0.0001 Not found Not found 0.380 \0.0001 93 Agriotes ustulatus 0.467 \0.0001 0.469 \0.0001 0.011 0.326 ‘‘Total plant damage’’ is number of missing plants due to wireworm feeding on seeds (seed damage) ? number of emerged plants damaged by wireworms (e.g. wilting of central leaves due to feeding on plant collars, broken central leaves)

Table 6 Percentage of fields where significant yield reductions Table 7 Maize grain yield (t/ha of grain at 14 % humidity) in a occurred at different densities of the Agriotes wireworm species being random subset of fields with \5 % (0.2 plants/m2) wireworm (A. studied (the average numbers of wireworms/trap were considered) sordidus Illiger) damage in untreated and treated plots with two dif- ferent maize hybrids in 2011 Wireworm Wireworm Fields Fields with Fields with species catches sampled yield yield Treatments/hybrids KORIMBOS DKC6677 (larvae/trap) (no.) reduction reduction (no.) (%) Untreated 11.19 13.40 Tefluthrin 11.34 N/A Agriotes 0 38 0 0.0 Clothiadinin N/A 13.49 ustulatus 0.1–1 25 0 0.0 Df/t/P 27/-0.550/0.587 21/-0.330/0.744 1.01–2 7 0 0.0 2.01–5 9 0 0.0 N/A unavailable data, Df/t/P degrees of freedom, t-value, P-value 5.01–10 9 1 11.1 >10.01 5 2 40.0 Agriotes 02100 Conclusion brevis 0.1–1 32 0 0.0 1.01–2 6 2 33.3 Theinformationhereinmaybeusedimmediatelytoimple- 2.01–5 7 4 57.1 ment IPM and to tackle soil pests attacking maize in many >5.01 3 1 33.3 European regions. As a result, it may lead to a considerable reduction in the use of soil pesticides and in a fall in the Agriotes 0 32 0 0.0 environmental impact of agriculture without negative reper- sordidus 0.1–1 83 0 0.0 cussions on farmers’ income. This can be achieved with the 1.01–2 10 0 0.0 procedure described in Furlan (2005): (i) locate the areas with >2.01 10 3 30.0 a serious risk of wireworm attacks by assessing field/envi- Bold values indicate the population levels that resulted in yield ronmental factors (Hermann et al. 2013; Furlan and Talon reduction 1997;Furlanetal.2011; Staudacher et al. 2013); (ii) in areas at risk of wireworm attacks, assess current Agriotes populations with the aforementioned procedure, i.e. use bait traps and pensating for stand reduction) may improve the correlation assess the actual average larval population, in fields intended between wireworm density and maize damage, as well as for maize sowing; (iii) if the average number of wireworms provide accurate (probably higher) thresholds for other does not exceed the thresholds established, maize may be groups of hybrids and for a range of conditions (e.g. irri- sown without any treatment; if the average number of wire- gated or non-irrigated fields). worms does exceed at least one of the thresholds, farmers have

123 J Pest Sci the option of moving maize to a no-risk field, as well as of Furlan L, To´th M, Yatsinin V, Ujvary I (2001a) The project to applying organic treatments (Furlan 2007;Furlanetal.2009b, implement IPM strategies against Agriotes species in Europe: what has been done and what is still to be done. Proceedings of 2010), or chemical treatments (Furlan et al. 2007, 2011 and XXI IWGO conference, Legnaro, 27 October–3 November Ferro and Furlan 2012). The aforementioned procedure may 2001:253–262 be considered the first reliable practical contribution towards Furlan L, Di Bernardo A, Maini S, Ferrari R, Boriani L, Boriani M, implementing IPM of wireworms in Europe in accordance Nobili P, Bourlot G, Turchi A, Vacante V, Bonsignore C, Giglioli G, To´th M (2001b) First practical results of click beetle trapping with EU Directive 2009/128/EC. with pheromone traps in Italy. Proceedings of XXI IWGO conference, Legnaro, 27 October–3 November 2001:253–262 Acknowledgments I would like to thank Mauro Davanzo, Franco Furlan L, Di Bernardo A, Boriani M (2002) Proteggere il seme di Fasan, Massimo Pasquon, Faustino Pintonello, Federico and Foresto mais solo quando serve. L’Informatore Agrario 8:131–140 Toffanin, and Ruggero Toffoletto for all of their support during the Furlan L, Canzi S, Toffoletto R, Di Bernardo A (2007) Effetti sul mais monitoring phase; thanks must also go to Alberto Sartori, Barbara della concia insetticida del seme. L’Informatore Agrario 5:92–96 Contiero, Francesca Chiarini, Manfredi Vale and Andrew Bailey for Furlan L, Caciagli P, Causin R, Di Bernardo A (2009a) Il seme di mais their statistical analyses and for revising the manuscript. va protetto solo quando serve. L’Informatore Agrario 5:36–44 Furlan L, Bonetto C, Costa B, Finotto A, Lazzeri L (2009b) Open Access This article is distributed under the terms of the Observations on natural mortality factors in wireworm popula- Creative Commons Attribution License which permits any use, dis- tions and evaluation of management options. IOBC/wprs Bull tribution, and reproduction in any medium, provided the original 45:436–439 author(s) and the source are credited. Furlan L, Bonetto C, Costa B, Finotto A, Lazzeri L, Malaguti L, Patalano G, Parker W (2010) The efficacy of biofumigant meals and plants to control wireworm populations. 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